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Host−parasite coevolution beyond the nestling stage? of host fledglings by the specialist screaming

María C. De Mársico, Mariela G. Gantchoff and Juan C. Reboreda

Proc. R. Soc. B 2012 279, 3401-3408 first published online 30 May 2012 doi: 10.1098/rspb.2012.0612

Supplementary data "Data Supplement" http://rspb.royalsocietypublishing.org/content/suppl/2012/05/24/rspb.2012.0612.DC1.h tml References This article cites 49 articles, 14 of which can be accessed free http://rspb.royalsocietypublishing.org/content/279/1742/3401.full.html#ref-list-1 Receive free email alerts when new articles cite this article - sign up in the box at the top Email alerting service right-hand corner of the article or click here

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Proc. R. Soc. B (2012) 279, 3401–3408 doi:10.1098/rspb.2012.0612 Published online 30 May 2012

Host–parasite coevolution beyond the nestling stage? Mimicry of host fledglings by the specialist Marı´aC.DeMa´rsico*, Mariela G. Gantchoff and Juan C. Reboreda Departamento de Ecologı´a, Gene´tica y Evolucio´n, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Pabello´n II, C1428EGA, Buenos Aires, Egg mimicry by obligate avian brood parasites and host rejection of non-mimetic eggs are well-known textbook examples of host–parasite coevolution. By contrast, reciprocal adaptations and counteradapta- tions beyond the egg stage in brood parasites and their hosts have received less attention. The screaming cowbird (Molothrus rufoaxillaris) is a specialist obligate whose fledglings look identical to those of its primary host, the (Agelaioides badius). Such a resemblance has been proposed as an adaptation in response to host discrimination against odd-looking young, but evidence supporting this idea is scarce. Here, we examined this hypothesis by comparing the survival rates of young screaming and non-mimetic shiny cowbirds (Molothrus bonariensis) cross-fostered to baywing nests and quantifying the similarity in plumage colour and begging calls between host and cowbird fledglings. Shiny cowbirds suffered higher post-fledging mortality rates (83%) than screaming cowbirds (0%) owing to host rejection. Visual modelling revealed that screaming cowbirds, but not shiny cowbirds, were indistinguishable from host young in plumage colour. Similarly, screaming cowbirds matched bayw- ings’ begging calls more closely than shiny cowbirds. Our results strongly support the occurrence of host fledgling mimicry in screaming cowbirds and suggest a role of visual and vocal cues in fledgling discrimi- nation by . Keywords: brood parasitism; mimicry; coevolution; chick rejection; visual modelling; cowbird

1. INTRODUCTION theoretical arguments that learned chick discrimination Exploitation of parental care by obligate avian brood would be maladaptive in hosts of evictor brood parasites parasites typically entails fitness costs to host parents. Para- such as [19] (see also [20]) and suggest that a coe- sitized nests may suffer partial or total brood losses owing volutionary arms race similar to that observed at the egg to the removal or destruction of host eggs by parasitic stage may also occur at the nestling stage [15–17] (but females [1–3], killing or eviction of host young by parasi- see [21]). Visual mimicry of host chicks has also been tic chicks [4,5], or increased mortality of host chicks reported in parasitic finches (Vidua sp.), whose young owing to competition within parasitized broods [6,7]. match precisely elaborate gape markings of host chicks These interactions between parasites and their hosts may [22,23]. Nevertheless, whether such a resemblance result in a coevolutionary arms race in which hosts evolve evolved in response to host rejection of alien chicks or defences against parasitism that, in turn, select for counter- through competition between host and parasitic young is defences in parasite populations [8,9]. A paradigmatic not yet clear [23,24]. example is the evolution of egg mimicry in parasitic females Reciprocal adaptations and counteradaptations beyond in response to host rejection of alien eggs, which has the nestling stage are even less documented [14]. In the been extensively studied in the common (Cuculus screaming cowbird (Molothrus rufoaxillaris), host fledgling canorus)[4,10–12]. mimicry has been proposed to explain the close resem- Beyond the egg stage, however, the occurrence of blance between parasitic fledglings and those of its coevolved adaptations between parasite and hosts has primary host, the baywing (Agelaioides badius)[25]. received less attention [13,14]. Some recent studies in Newly hatched screaming cowbirds and baywings differ bronze-cuckoos (Chalcites spp. and Chrysococcyx minutillus) minimally in skin and bill coloration but as parasitic and their hosts have shown that host parents were able to chicks grow older, they become increasingly similar to reject parasitic chicks either through the desertion of para- host chicks [26]. By the time they leave the nest, screaming sitized nests soon after hatching [15] or active eviction of cowbirds and baywings look nearly identical to the human parasitic young out of the nest [16,17], and later work eye, and this resemblance persists until cowbird juveniles suggests that host rejection behaviour, in turn, may have begin to moult into the adult black plumage, about five selected for reciprocal host chick mimicry in bronze- weeks after hatching [27,28]. The appearance of screaming cuckoos [15,18]. These findings have challenged prior cowbird juveniles cannot be attributed to common descent [29], thus it has been proposed as a case of visual mimicry driven by host rejection of odd-looking young soon after * Author for correspondence ([email protected]). fledging [25]. This idea was based on the observation Electronic supplementary material is available at http://dx.doi.org/ that non-mimetic juveniles of another brood parasite, 10.1098/rspb.2012.0612 or via http://rspb.royalsocietypublishing.org. the (Molothrus bonariensis), fledged from

Received 15 March 2012 Accepted 3 May 2012 3401 This journal is q 2012 The Royal Society Downloaded from rspb.royalsocietypublishing.org on July 26, 2012

3402 M. C. De Ma´rsico et al. Fledgling mimicry in screaming cowbirds

Table 1. Brood composition at fledging of eight breeding groups of baywings observed over a week after fledging. (Figures indicate number of fledglings of each ; bw, baywing; scr, screaming cowbird; sh, shiny cowbird. The last column summarizes the observations of non-mimetic shiny cowbird fledglings. All baywing (n ¼ 21) and screaming cowbird fledglings (n ¼ 6) were found alive by the end of the observation period.) group bw scr sh fate of shiny cowbird fledgling

1 1 0 1 survived, fed by individuals other than the foster parents 2 5 0 1 not fed by baywings, found dead on the ground near the nest on day 2 after fledging 3 4 1 1 not fed by baywings on day 1 post-fledging, ‘vanished’ on day 2 4220 5 0 0 1 fed by a baywing on day 1 post-fledging, found alone on day 2, ‘vanished’ on day 3 6 4 1 1 not fed by baywings on days 1 and 2 post-fledging, ‘vanished’ on day 3 7 4 1 1 not fed by baywings on day 1 post-fledging, ‘vanished’ on day 2 8110 baywing nests but experienced high post-fledging mortality than 200 species throughout its distribution and uses bayw- rates, presumably because baywings no longer feed them ings as secondary hosts [4,25]. once they leave the nest [25]. Shiny cowbird fledglings To assess baywings’ response towards young that do not resemble hosts and screaming cowbirds in size and body resemble their own, we artificially parasitized 53 baywing shape but lack the rufous plumage coloration characteristic nests (from a sample of 193 nests) with a single shiny cowbird of baywings [28]. However, further evidence in support egg (n ¼ 50) or hatchling (n ¼ 3) collected from nearby nests of host discrimination against odd-looking juveniles is of chalk-browed mockingbirds (Mimus saturninus). Artificially lacking, as are objective assessments of the degree of simi- parasitized broods were not further manipulated because we larity between screaming cowbird and host young. Avian aimed to determine survival rates of shiny cowbird chicks visual systems differ markedly from that of humans [30], under the most realistic conditions in baywing nests. Shiny thus quantifying plumage similarity between hosts and cowbird and screaming cowbird nestlings typically hatched parasites from an avian perspective is necessary to better one day before host chicks (incubation periods: 13 days for understand the evolution of mimicry in host–parasite sys- baywings, and 12 days for shiny and screaming cowbirds). tems [11,12,18,31,32]. In addition, hosts may use vocal We estimated survival rates of host and parasite chicks from cues to discriminate between their own and alien young, 34 nests (10 unparasitized, 12 parasitized by screaming cow- which may select for mimetic begging calls in brood only, six parasitized by screaming/shiny cowbirds and six parasite chicks [15]. Although prior observations suggest parasitized by shiny cowbird only) that either survived to that vocal mimicry may occur in screaming cowbirds fledging (n ¼ 33) or failed owing to causes other than nest pre- [25], the similarity in begging call structure between dation (the entire brood died as a result of heavy ectoparasite screaming cowbird and host nestlings and fledglings has infestation, n ¼ 1). not yet been analysed. Nests were checked every 1–2 days. We marked chicks Our aim in this study was to evaluate the occurrence with permanent ink and assigned them to baywing, scream- of host fledgling mimicry in screaming cowbirds. We ing or shiny cowbird using skin and bill coloration as conducted a cross-fostering experiment in order to test diagnostic cues [26]. We weighed all chicks daily or every whether post-fledging survival rates differ between ‘non- other day in order to build growth curves, which are pub- mimetic’ (shiny cowbird) and ‘mimetic’ (screaming lished elsewhere [33]. These data show that shiny cowbirds cowbird) fledglings reared by baywings, and quantified in baywing nests grew faster than host young and reached a how well screaming cowbirds match host fledglings in higher asymptotic body mass, comparable to that of shiny plumage colour and begging calls using avian visual cowbird chicks reared by their primary hosts in the same modelling and multivariate techniques. study area [33]. At the age of 10–11 days, host and parasite chicks were banded with a unique combination of colour plastic leg bands and a numbered aluminium band. We mon- 2. MATERIAL AND METHODS itored nests from a distance daily or every other day to (a) Study site and field methods determine the date at which chicks fledged (average fledging The study was conducted at ‘Reserva El Destino’ (358080 S, age: 14 days post-hatching [33]). 578230 W) in the province of Buenos Aires, Argentina, We estimated survival rates of host and parasitic fledglings between 2002 and 2007. Baywings breed in the area from during the breeding seasons of 2005–2006 and 2006–2007 December to February using domed nests of other bird by following eight groups of adults with colour-banded species (e.g. Annumbius annumbis, Phacellodomus spp., fledglings over a week after fledging (table 1). From these, Synallaxis spp.), secondary cavities and nest-boxes (see the six were artificially parasitized with a single shiny cowbird electronic supplementary material for details). Screaming egg (n ¼ 4) or hatchling (n ¼ 2), whereas the remaining two cowbirds and shiny cowbirds are year-round residents were naturally parasitized by screaming cowbirds and left in the area and annually parasitize roughly 91–97% and unmanipulated. All groups parasitized by shiny cowbirds 7–25% of baywing nests, respectively [33]. The screaming and one of those parasitized solely by screaming cowbirds cowbird is the most specialized parasitic cowbird with only had at least one helper at the nest in addition to the breeding three known host species so far; it parasitizes almost exclu- pair. These groups remained in the vicinity (less than 200 m) sively the baywing in most of its geographical range of their nesting sites and were located through alarm calls of [25,34]. By contrast, the shiny cowbird parasitizes more adults and begging calls of young. We conducted focal

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Fledgling mimicry in screaming cowbirds M. C. De Ma´rsico et al. 3403 observations on each group once a day until every fledgling indistinguishable, and values of more than 1.0 indicate that within the group was located and its identity recorded using two spectra would be increasingly easy to discriminate [42,43]. 8 40 binoculars. Fledglings that were not found by the end of the first week after fledging despite exhaustive search- (c) Sampling of begging calls ing within the group’s territory were considered to be dead. We recorded begging calls of 13 baywing, 13 screaming cow- Shiny cowbird fledglings gave loud and distinctive begging bird and 15 shiny cowbird fledglings in captivity between calls that made them conspicuous and easy to locate even 13 and 20 days post-hatching (average: 16.1 + 0.4 days). when hidden in the surrounding vegetation. Thus, we are con- Recordings were made using a directional microphone Senn- fident that all shiny cowbird fledglings still alive were sighted heiser ME 66 connected to a digital audio recorder Edirol R- during our observations. 09, at a sampling rate of 44.1 kHz stereo (16 bits), and saved as standard wav files. Prior to recording, fledglings were fed to satiation and then deprived of food for 60 min to standardize (b) Sampling of plumage reflectance and their hunger level. Subsequently, we isolated them visually visual modelling and acoustically from other fledglings and recorded their We analysed the degree of similarity in plumage coloration begging calls during 3–5 min. Sound files were converted to among 14 screaming cowbird, 25 shiny cowbird and 15 bayw- sonograms using RAVEN PRO v. 1.3 (Cornell Bioacoustics ing fledglings born in the study area during the breeding season Research Program, Ithaca, NY, USA) with a Hanning 2009–2010. Baywing and cowbird chicks were removed window of 256 samples and 248 Hz filter bandwidth, a time from nests at the age of 8–10 days, taken to the laboratory grid with hop size of 128 samples and 50 per cent overlap, and hand-reared to nutritional independence (see the and a frequency grid with discrete Fourier transform size of electronic supplementary material for details). 256 samples and grid spacing of 172 Hz. Call bouts were We measured fledglings’ plumage reflectance on eight body defined as repetitions of syllables with a discrete beginning regions (crown, throat, breast, upper and lower back, rump, and end in the sonogram. For each host and cowbird fledgling, outer wing coverts and primary feathers; see the electronic sup- we measured the maximum and minimum frequency (kHz), plementary material) between days 13 and 20 post-hatching peak frequency (kHz), frequency bandwidth (kHz), call dur- (average age: 16.1 + 0.4 days). Reflectance measurements ation (s) and number of syllables from sonograms (see the were taken indoors using an Ocean Optics S2000 spectrometer electronic supplementary material for details). Measurements with a PX-2 pulsed xenon light source and a bifurcated fibreop- were taken of each of the first 10 call bouts following the initial tic probe (Ocean Optics, Inc.). The probe was housed in a black 60 s of recording and then averaged for each individual. The plastic tube to minimize incident ambient light and hold the shiny cowbird sample included fledglings reared by baywings probe tip at a constant distance (19.0+ 0.1 mm) and angle and other host species (see the electronic supplementary (908) from the body surface. Reflectance measures were cali- material for details). However, a prior study failed to find sig- brated against a white standard of barium sulphate [35], and nificant differences in begging call structure between shiny against a black standard with the light source off. Calibration cowbirds reared by different host species in our study area was performed immediately before measuring each individual (R. Gloag 2010, unpublished data). These results suggest a in order to minimize any error owing to light source or sensor minor role of learning in shaping the begging call structure drift. We obtained data via spectral acquisition software of shiny cowbird young that could have obscured the interpretation of our results. package OOIBASE32 (Ocean Optics, Inc.). We used the Vorobyev–Osorio colour discrimination (d) Statistical analysis model [36,37] to calculate discriminability for each pair of We ran two-tailed one-sample t-tests to analyse whether homologous body regions of baywing, screaming and shiny mean chromatic differences between each pair of species sig- cowbird fledglings. The model calculates a distance in nificantly differ from the discrimination threshold of 1 jnd. avian colour space (DS) defined by the quantum catches of To remove the problem of non-independence of pairwise each cone cell type in the avian retina. Calculation of quan- chromatic distances in statistical tests, we first compared tum catches requires data on spectral sensitivities and the each individual host and parasitic fledgling with all fledglings relative number of each cone cell type in the receiver’s of a given species to calculate a mean chromatic distance, retina. These data are unavailable for baywings, but current unique to each host or parasitic fledgling [18]. These evidence suggests that spectral sensitivities of photoreceptors means were the unit of analyses in t-tests. are highly conserved among non-corvid songbirds [30,38]. We performed a discriminant function analysis to assess Therefore, we used data from the blue tit (Cyanistes caeruleus) how the parameters extracted from begging calls discriminate as representative of the baywing’s visual system [18,30]. between baywing, screaming and shiny cowbird fledglings. Cone cell type ratios, however, vary among species [30]. The analysis followed a stepwise procedure in which the vari- Thus, in order to assess sensitivity of our results to different able that minimizes the overall Wilk’s lambda was entered at single cone ratios, we calculated quantum catches using data each step. Statistical analyses were performed using SPSS from the blue tit, blackbird (Turdus merula) and European v. 19 (IBM, Chicago, IL, USA) and STATVIEW v. 5.0 (SAS starling (Sturnus vulgaris), which encompasses known vari- Institute). Tests were two-tailed with an alpha level of 0.05. ation among [30,39]. Results were qualitatively identical, thus we reported DS values generated using blue (e) Ethical considerations tit data. Calculations were performed using the SPEC pack- Experimental cross-fostering of shiny cowbird chicks was age in R [40,41] for standard d65 daylight illumination. The necessary to conduct this study given the low rates of natural output of the model is in terms of just noticeable differences parasitism by shiny cowbirds in baywing nests. Failure rates (jnds), where 1.0 jnd means that two spectra are barely dis- of baywing nests are typically high (approx. 80%) in the tinguishable under ideal viewing conditions. Values of DS study area, mainly owing to nest or abandonment less than 1.0 mean that two spectra would be in response to multiple parasitism. Thus, we needed to

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3404 M. C. De Ma´rsico et al. Fledgling mimicry in screaming cowbirds

(a)

* (b) 2.0 *

* 1.5 * *

1.0 n.s.

chromatic distance (jnds) 0.5

0 crown throat breast upper lower rump primary outer back back feathers coverts Figure 1. (a) Baywing, screaming cowbird and shiny cowbird fledglings (from left to right), illustrating juvenile plumage color- ation. (b) Mean + s.e. chromatic distances (DS) in terms of just noticeable differences (jnds) between baywings and screaming cowbirds (white bars), baywings and shiny cowbirds (grey bars), and screaming and shiny cowbirds (black bars). Intraspecific contrasts among host fledglings are given for comparison (stripped white bars). The dashed line indicates the discrimination threshold of 1 jnd. Asterisks indicate mean chromatic distances significantly larger than 1 jnd after one-sample t-tests (p , 0.05); n.s. indicates mean contrasts not significantly different from 1 jnd. Sample sizes were: 15 baywing, 14 screaming cowbird and 25 shiny cowbird juveniles. parasitize a relatively large number of nests in order to get esti- fledglings were alone and begging repeatedly perched on mates of post-fledging survival rates. However, as we observed trees or on the ground within their natal territories the that most cross-fostered chicks died after leaving the nest we last day we observed them alive. discontinued the experiment, limiting our sample to six artifi- cially parasitized nests that fledged shiny cowbird young. (b) Visual and vocal similarity between host and parasitic fledglings 3. RESULTS Screaming cowbird and baywing fledglings were almost (a) Survival of mimetic and non-mimetic young identical in appearance to human eyes (figure 1a), and Chick survival rates in nests that were not depredated were results of visual modelling indicated that they were also 91 per cent for baywings (n ¼ 33 nests), 94 per cent indistinguishable from an avian perspective. Mean chro- for screaming cowbird (n ¼ 18 nests) and 92 per cent for matic distances between plumage spectra of screaming shiny cowbird chicks (n ¼ 12 nests). ‘Non-mimetic’ cowbird and host juveniles were significantly below the dis- (shiny cowbird) and ‘mimetic’ (screaming cowbird) crimination threshold (figure 1b). Interestingly, screaming chicks fledged successfully in all but one nest where the cowbird fledglings were visually not different from host entire brood died as a result of heavy infestation with nest fledglings than host fledglings were from each other in mites. Overall, 11 of 12 shiny and 30 of 31 screaming most plumage patches (figure 1b). Shiny cowbird fledglings, cowbird chicks survived to fledging in baywing nests. on the other hand, varied in appearance from both scream- By contrast, post-fledging survival rates differed mark- ing cowbirds and baywings (figure 1a). Mean chromatic edly between ‘mimetic’ and ‘non-mimetic’ young. distances between shiny cowbirds and the other two species Although all host and screaming cowbird fledglings were were consistently larger than the corresponding distances found alive a week after nest departure, only one of between screaming cowbirds and baywings and exceeded six shiny cowbird fledglings survived the same period the discrimination threshold in primary feathers and outer (table 1). We did not see baywings escorting or feeding wing coverts (figure 1b). Mean chromatic distance between this one shiny cowbird, but we repeatedly observed two shiny and screaming cowbirds for the crown plumage patch individuals of another species (Cychlaris gujanensis) deliver- was also above the threshold (figure 1b). ing food to it. From the remaining five shiny cowbird Screaming cowbirds matched baywing’s begging fledglings, one was found dead on the ground near the calls more closely than shiny cowbirds (table 2 and nest on day 2 post-fledgling and the other four were not figure 2a,b). The discriminant function analysis classified longer seen after 48–72 h outside the nest. These missing the begging calls of baywings, screaming cowbirds and

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Fledgling mimicry in screaming cowbirds M. C. De Ma´rsico et al. 3405

baywing screaming cowbird shiny cowbird (a) 20 16 12 8 4 frequency (kHz) frequency

0 0.1 0.2 0.3 0.10 0.2 0.3 0.4 0.10 0.2 0.3 0.4 0.5 time (s)time (s) time (s)

(b) 3

2

1 scr

0 sh bw –1

discriminant function 2 –2

–3 –4 –2 0 2468 discriminant function 1 Figure 2. (a) Representative sonograms of begging calls of host and parasite fledglings and (b) canonical plots from discrimi- nant function analysis separating the begging calls of baywing (open circles), screaming cowbird (filled circles) and shiny cowbird (black triangles). Black stars indicate the centroid of each group labelled bw, scr and sh, respectively. Sample sizes were: 13 baywing, 13 screaming cowbird and 15 shiny cowbird fledglings.

Table 2. Begging call parameters (mean + 1 s.e.) of baywing (bw), screaming cowbird (scr) and shiny cowbird (sh) fledglings. (The last two columns show the standardized coefficients for each parameter for each discriminant function (see §2). Only peak frequency, number of syllables and call duration entered the discriminant analysis.) call parameter bw (n ¼ 13) scr (n ¼ 13) sh (n ¼ 15) function 1 function 2 min frequency (kHz) 5.71 + 0.25 4.67 + 0.12 5.19 + 0.33 max frequency (kHz) 8.48 + 0.35 7.66 + 0.21 8.96 + 0.21 bandwidth (kHz) 2.78 + 0.23 2.99 + 0.17 3.77 + 0.37 peak frequency (kHz) 7.26 + 0.20 6.23 + 0.14 7.67 + 0.15 0.15 1.00 number of syllables 3.18 + 0.27 3.32 + 0.28 10.2 + 0.59 1.90 20.71 call duration (s) 0.18 + 0.02 0.18 + 0.02 0.37 + 0.02 21.22 0.60 shiny cowbirds with 86 per cent, 86 per cent and 100 per fledglings, suggesting that female and male baywings cent accuracy respectively, using the number of syllables, use similar rejection rules. This contrasts with prior peak frequency and call duration (Wilks’ l ¼ 0.082, exact studies on the superb fairy-wren (Malurus cyaneus) para- F: F6,72 ¼ 29.8, p , 0.001; figure 2b). The number of syl- sitized by Horsfield’s bronze-cuckoos (Chalcites basalis) lables and call duration distinguished between shiny and the shining bronze-cuckoo (Chalcites lucidus), where cowbirds and the other two species, whereas peak fre- apparently only host females showed discrimination quency distinguishes between baywing and screaming behaviour against parasitic young [15,44]. cowbirds (table 2 and figure 2b). The latter resemble bayw- Increased post-fledging mortality as a consequence of ing begging calls in number of syllables and duration but host discrimination seems the most likely explanation for uttered lower pitched calls. shiny cowbird fledglings ‘vanishing’ after leaving the nest, as they have limited flying skills and are nutritionally depen- dent on their host parents for several weeks. Although 4. DISCUSSION adoption of parasitic fledglings by individuals other than This study supports the idea that screaming cowbirds the foster parents is possible ([45], this study), this is a mimic the juveniles of its primary host, the baywing. rare phenomenon that cannot account for the consistent Cross-fostering experiments of shiny cowbird chicks disappearance of shiny cowbirds fledged from baywing showed that baywings successfully reared non-mimetic nests. Likewise, it seems unlikely that cross-fostering per chicks, but they stopped providing parental care to them se had an effect on host’s behaviours towards screaming after fledging. Furthermore, our observations indicated and shiny cowbird fledglings given that this manipulation that both host parents refused to feed shiny cowbirds was performed early in the egg or nestling stages; well in

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3406 M. C. De Ma´rsico et al. Fledgling mimicry in screaming cowbirds advance hosts began to show rejection behaviour towards [24,49]. Both alternatives are compatible with our results, cross-fostered young. In addition, the results of visual mod- and more data are needed to assess their relative im- elling indicated that, from an avian perspective, screaming portance as selective forces driving the resemblance of cowbird but not shiny cowbird fledglings were indistin- screaming cowbirds to baywing young. guishable from those of baywings on the basis of plumage Screaming cowbirds and baywings also bore a closer coloration. These findings, in agreement with prior obser- vocal resemblance than baywings and shiny cowbirds. vations [25], strongly suggest that the host-like Screaming cowbirds matched the begging calls of host appearance of screaming cowbird juveniles is adaptive juveniles in all parameters analysed but gave lower fre- and evolved in response to host discrimination against quency calls, a difference that might be partly owing to odd-looking young after fledging. the parasite’s larger body size [33,50]. These results sup- Coevolved adaptations beyond the egg stage between port the early suggestion that mimicry of host fledglings brood parasites and their hosts have been investigated by screaming cowbirds may extend also to vocal cues relatively little, partly because theory predicts evolution- [25], though similarity does not necessarily imply mimicry ary constraints on learned chick discrimination in the [51]. Vocal resemblance by parasitic chicks has been pre- hosts of evictor brood parasites such as cuckoos [19]. viously reported in various cuckoo species [15,52,53], This traditional view, however, has been challenged by and available evidence indicates that it may be socially recent evidences of a coevolutionary arms race at the acquired, as cross-fostered parasite chicks modified the nestling stage between bronze-cuckoos and their hosts structure of their begging calls to match more closely that [15–17]. On the other hand, there are no theoretical con- of the host that raised them [52,53]. Whether host-like beg- straints to the possibility of nestling rejection when hosts ging calls in screaming cowbirds are innate or socially are exploited by non-evictor or ‘nest-mate tolerant’ acquired remains an open question. Pilot observations, brood parasites such as cowbirds [19]. Nevertheless, however, showed that screaming cowbird fledglings exper- clear-cut examples of host discrimination against non- imentally cross-fostered to chalk-browed mockingbird evictor parasites are still relatively scarce [13]. Our nests displayed similar begging calls to those raised by findings that baywings discriminate against non-mimetic baywings and were able to attract the attention of adult parasitic young after they leave the nest extend these baywings from nearby territories (M. C. De Ma´rsico prior results and show that host–parasite coevolution 2011, unpublished data). These observations suggest that may occur even at the fledgling stage. the begging call structure of screaming cowbirds might be The evolution of parasite chick rejection so late in the at least partially genetically determined and may play a breeding cycle is puzzling as, by the time of fledging, host role in attracting host attention after leaving the nest. parents have already paid much of the costs of parasitism Our results support the hypothesis that screaming cow- [25]; at this late stage, the potential costs of erroneously bird fledglings exhibit both visual and vocal similarity to rejecting one’s own offspring (recognition errors) might their primary host, the baywing, and strongly suggest that be expected to outweigh any benefit of rejection behav- such a resemblance makes them mimetic to host fledglings, iour [46]. Furthermore, during the late nestling and probably driven by host discrimination against non-mimetic fledgling periods, baywings often have helpers at the juveniles. Future research should aim to assess the fitness nest that contribute to young provisioning and may payoffs of post-fledging parental care to baywings and reduce the costs to host parents of raising parasitized the relative importance of visual and vocal cues in host broods to independence [47,48]. In theory, hosts may discrimination in order to improve our understanding of evolve defences against parasitic young either when para- the evolution of this last line of host defence. sites have broken down earlier lines of defence [15]or The manipulations performed in this work comply with the when they are constrained from evolving defences against current laws of Argentina. parasite eggs [17]. In baywings, the evolution of fledgling discrimination in the absence of rejection behaviour We thank Fundacio´n Elsa Shaw de Pearson for permitting against parasite eggs and nestlings suggests that they us to conduct this study at Reserva El Destino, and might be prevented from reliably discriminating against C. Ursino, V. Fiorini and A. de la Colina for helping us with parasitic eggs or chicks [25]. Baywings breed in close, chick collection and hand rearing. We are grateful to C. Facchinetti, R. Gloag and D. Lijtmaer for advice in data dark nests where host and parasitic chicks are often analysis; R. Gloag, B. Mahler, J. Sapp and two anonymous crowded and might be difficult to distinguish from each reviewers for helpful comments on earlier drafts. M.C.D.M. other on the basis of visual or vocal cues. Under this scen- was supported by a fellowship from the Consejo Nacional de ario, rejection of parasitic fledglings may still be selectively Investigaciones Cientı´ficas y Te´cnicas (CONICET). J.C.R. is advantageous to host parents if they avoid prolonged par- a Research Fellow of CONICET. This work was supported ental care of unrelated offspring and improve their by grants of Agencia Nacional de Promocio´n Cientı´fica prospects for future survival or reproduction [5]. An y Tecnolo´gica and University of Buenos Aires. alternative explanation is that rejection behaviour in baywings is the expression of host’s pre-existing prefer- ences for fledglings exhibiting visual or vocal traits that REFERENCES signal species identity, rather than an adaptation in 1 Davies, N. B. & Brooke, M. de L. 1988 Cuckoos versus reed warbler hosts: adaptations and counteradaptations. response to fitness costs of parasitism at the fledging Anim. Behav. 36, 262–284. (doi:10.1016/S0003-3472 stage. 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